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Infectious virus in exhaled breath of symptomatic seasonal influenza cases from a college community

Jing Yan, Michael Grantham, Jovan Pantelic, P. Jacob Bueno de Mesquita, Barbara Albert, Fengjie Liu, Sheryl Ehrman, View ORCID ProfileDonald K. Milton, for the EMIT Consortium
doi: https://doi.org/10.1101/194985
Jing Yan
aMaryland Institute for Applied Environmental Health, School of Public Health, University of Maryland, College Park, MD, 20742
bDepartment of Chemical and Biomolecular Engineering, Clark School of Engineering, University of Maryland, College Park, MD, 20742
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Michael Grantham
aMaryland Institute for Applied Environmental Health, School of Public Health, University of Maryland, College Park, MD, 20742
cCurrent address: Department of Biology, Missouri Western State University, St. Joseph, MO 64507
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Jovan Pantelic
aMaryland Institute for Applied Environmental Health, School of Public Health, University of Maryland, College Park, MD, 20742
dCurrent address: Center for the Built Environment, University of California Berkeley, Berkeley, CA 94720
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P. Jacob Bueno de Mesquita
aMaryland Institute for Applied Environmental Health, School of Public Health, University of Maryland, College Park, MD, 20742
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Barbara Albert
aMaryland Institute for Applied Environmental Health, School of Public Health, University of Maryland, College Park, MD, 20742
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Fengjie Liu
aMaryland Institute for Applied Environmental Health, School of Public Health, University of Maryland, College Park, MD, 20742
eCurrent address: Division of Viral Products, Center for Biologics Evaluation and Research (CBER), FDA, Silver Spring, MD, 20903
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Sheryl Ehrman
bDepartment of Chemical and Biomolecular Engineering, Clark School of Engineering, University of Maryland, College Park, MD, 20742
fCurrent address: Davidson College of Engineering, San José State University, San José, CA 95192
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Donald K. Milton
aMaryland Institute for Applied Environmental Health, School of Public Health, University of Maryland, College Park, MD, 20742
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  • ORCID record for Donald K. Milton
  • For correspondence: dmilton@umd.edu
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Abstract

Little is known about the amount and infectiousness of influenza virus shed into exhaled breath. This contributes to uncertainty about the importance of airborne influenza transmission. We screened 355 symptomatic volunteers with acute respiratory illness and report 142 cases with confirmed influenza infection who provided 218 paired nasopharyngeal (NP) and 30-minute breath samples (coarse >5 μm and fine <5 μm fractions) on days 1 to 3 post symptom onset. We assessed viral RNA copy number for all samples and cultured NP swabs and fine aerosols. We recovered infectious virus from 52 (39%) of the fine aerosols and 150 (89%) of the NP swabs with valid cultures. The geometric mean RNA copy numbers were 3.8×104/30-min fine, 1.2×104/30-min coarse aerosol sample, and 8.2×108 per NP swab. Fine and coarse aerosol viral RNA was positively associated with body mass index (fine p<0.05, coarse p<0.10) and number of coughs (fine p<0.001, coarse p<0.01) and negatively associated with increasing days since symptom onset (fine p<0.05 to p<0.01, coarse p<0.10) in adjusted models. Fine aerosol viral RNA was also positively associated with having influenza vaccination for both the current and prior season (p<0.01). NP swab viral RNA was positively associated with upper respiratory symptoms (p<0.01) and negatively associated with age (p<0.01) but was not significantly associated with fine or coarse aerosol viral RNA or their predictors. Sneezing was rare, and sneezing and coughing were not necessary for infectious aerosol generation. Our observations suggest that influenza infection in the upper and lower airways are compartmentalized and independent.

Significance Lack of human data on influenza virus aerosol shedding fuels debate over the importance of airborne transmission. We provide overwhelming evidence that humans generate infectious aerosols and quantitative data to improve mathematical models of transmission and public health interventions. We show that sneezing is rare and not important for, and that coughing is not required for influenza virus aerosolization. Our findings, that upper and lower airway infection are independent and that fine particle exhaled aerosols reflect infection in the lung, open a new pathway for understanding the human biology of influenza infection and transmission. Our observation of an association between repeated vaccination and increased viral aerosol generation demonstrated the power of our method, but needs confirmation.

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  • ↵2 Membership of the EMIT Consortium is provided in the Supporting Information

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Posted January 03, 2018.
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Infectious virus in exhaled breath of symptomatic seasonal influenza cases from a college community
Jing Yan, Michael Grantham, Jovan Pantelic, P. Jacob Bueno de Mesquita, Barbara Albert, Fengjie Liu, Sheryl Ehrman, Donald K. Milton, for the EMIT Consortium
bioRxiv 194985; doi: https://doi.org/10.1101/194985
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Infectious virus in exhaled breath of symptomatic seasonal influenza cases from a college community
Jing Yan, Michael Grantham, Jovan Pantelic, P. Jacob Bueno de Mesquita, Barbara Albert, Fengjie Liu, Sheryl Ehrman, Donald K. Milton, for the EMIT Consortium
bioRxiv 194985; doi: https://doi.org/10.1101/194985

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